The Digestive Tract As an Essential Organ for Water Acquisition in Marine Teleosts: Lessons from Euryhaline Eels Yoshio Takei

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The Digestive Tract As an Essential Organ for Water Acquisition in Marine Teleosts: Lessons from Euryhaline Eels Yoshio Takei Takei Zoological Letters (2021) 7:10 https://doi.org/10.1186/s40851-021-00175-x REVIEW Open Access The digestive tract as an essential organ for water acquisition in marine teleosts: lessons from euryhaline eels Yoshio Takei Abstract Adaptation to a hypertonic marine environment is one of the major topics in animal physiology research. Marine teleosts lose water osmotically from the gills and compensate for this loss by drinking surrounding seawater and absorbing water from the intestine. This situation is in contrast to that in mammals, which experience a net osmotic loss of water after drinking seawater. Water absorption in fishes is made possible by (1) removal of monovalent ions (desalinization) by the − esophagus, (2) removal of divalent ions as carbonate (Mg/CaCO3) precipitates promoted by HCO3 secretion, and (3) facilitation of NaCl and water absorption from diluted seawater by the intestine using a suite of unique transporters. As a result, 70–85% of ingested seawater is absorbed during its passage through the digestive tract. Thus, the digestive tract is an essential organ for marine teleost survival in the hypertonic seawater environment. The eel is a species that has been frequently used for osmoregulation research in laboratories worldwide. The eel possesses many advantages as an experimental animal for osmoregulation studies, one of which is its outstanding euryhalinity, which enables researchers to examine changes in the structure and function of the digestive tract after direct transfer from freshwater to seawater. In recent years, the molecular mechanisms of ion and water transport across epithelial cells (the transcellular route) and through tight junctions (the paracellular route) have been elucidated for the esophagus and intestine. Thanks to the rapid progress in analytical methods for genome databases on teleosts, including the eel, the molecular identities of transporters, channels, pumps and junctional proteins have been clarified at the isoform level. As 10 y have passed since the previous reviews on this subject, it seems relevant and timely to summarize recent progress in research on the molecular mechanisms of water and ion transport in the digestive tract in eels and to compare the mechanisms with those of other teleosts and mammals from comparative and evolutionary viewpoints. We also propose future directions for this research field to achieve integrative understanding of the role of the digestive tract in adaptation to seawater with regard to pathways/mechanisms including the paracellular route, divalent ion absorption, metabolon formation and cellular trafficking of transporters. Notably, some of these have already attracted practical attention in laboratories. (Continued on next page) Correspondence: [email protected] All transporters have both common names and those derived from the solute carrier (SLC) family. In this review, the SLC family names are shown in addition to the common names at first appearance to indicate similar transport characteristics and susceptibility to common inhibitors. The number after the common name is not hyphenated, and the acronyms are capitalized (e.g., PAT1). Laboratory of Physiology, Department of Marine Bioscience, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Takei Zoological Letters (2021) 7:10 Page 2 of 34 (Continued from previous page) Keywords: Osmoregulation, Seawater adaptation, Anguilla spp., Esophageal desalinization, Biomineralization, Epithelial transport, Transcellular transport, Paracellular transport, Tight junction protein, Hormonal regulation, Metabolon, Vesicle trafficking 1. Background ionoregulators and osmoconformers). Thus, they need only 1.1 Diverse body fluid regulation in marine fishes to excrete excess ions and retain urea at the kidneys, as os- Extant vertebrates inhabit three different types of habi- motic forces on water diffusion are nearly abolished. Mar- tats in terms of osmoregulation: water- and ion-deficient ine teleosts use a third strategy like that of marine land habitats, water-sufficient and ion-deficient inland mammals, birds and reptiles, which have plasma ion con- freshwater (FW) habitats, and water- and ion-sufficient centrations and osmolality approximately one-third that of seawater (SW) habitats. Because of the high osmolality SW (making them iono- and osmoregulators) (Fig. 1). of SW, however, the ocean is generally a desiccative en- Thus, they must counter osmotic water loss and excess ion vironment for marine teleost fishes. To address this gain. To address this hydromineral challenge, marine tele- issue, marine fishes use three different strategies for osts drink SW and absorb water together with ions in the body fluid regulation (Fig. 1). The first strategy is intestine. Ions also enter the body via the body surfaces adopted by the most primitive extant vertebrate group, driven by their concentration gradients. Then, excess the hagfishes, which conform their plasma to environ- monovalent ions are excreted mostly by the gills, and excess mental SW in terms of both ion concentrations and divalent ions are excreted by the kidneys [127, 144]. osmolality (acting as iono- and osmoconformers), similar Gill ionocytes (mitochondrion-rich cells) are respon- − to marine invertebrates (Fig. 1). Thus, they exert little sible for active Na+ and Cl excretion (see [36, 51]). As osmoregulation effort and incur little expense. The ions acquisition of ionocytes appeared to be one of the cues − involved are monovalent ions (Na+ and Cl ), as divalent for teleosts to re-enter the marine environment after the 2+ 2− ions (Mg and SO4 ) are maintained at levels lower teleost-specific whole-genome duplication that occurred than those in plasma [63]. The second strategy is ca. 300 mya [91], gill ionocytes have been the most in- employed by elasmobranchs and a lobe-finned bony fish, tensively studied tissue in osmoregulation research. Con- the coelacanth, whose plasma ion concentrations are sequently, the molecular mechanisms of transcellular lower than the concentrations in SW but whose plasma and paracellular ion transport have been elucidated, and osmolality is maintained at a level similar to that in SW via these mechanisms have been summarized in several re- accumulation of urea in the plasma (acting as views (e.g., [30, 85, 86, 90]). SW contains high Fig. 1 Diverse strategies for adaptation of fishes to a hypertonic seawater environment. The ion concentrations are in mM, and osmolality (Osm) is in mOsm/l. The values for eels are for eels acclimated to seawater. The values for seawater are shown in Table 1. All marine mammals, birds and reptiles are iono- and osmoregulators, while the only amphibian that can acclimate to seawater, the crab-eating frog (Fejervarya cancrivora), is an ionoregulator and osmoconformer, as are elasmobranchs. Illustrated by Mari Kawaguchi of Sophia University (https://www.ginganet.org/mari) Takei Zoological Letters (2021) 7:10 Page 3 of 34 2+ 2− concentrations of the divalent ions Mg and SO4 in mammals are usually lower than SW NaCl concentra- addition to monovalent ions (Table 1), and the sites of tions, water is further lost in the urine for NaCl excre- MgSO4 excretion are the proximal tubules of the kidneys tion. Although there is a report showing that whale − [18, 19]. Transporters involved in transcellular Mg2+ kidneys can concentrate Cl to a concentration of 820 transport have been suggested to exist in the euryhaline mM [189], urine NaCl concentrations are usually much pufferfish mefugu, Takifugu obscurus [96, 97], and those lower than SW concentrations [20]. Marine birds and 2− for SO4 transport have been proposed to exist in the reptiles possess salt glands that concentrate NaCl above mefugu [107]andeel[256]. However, the whole picture of SW levels through a mechanism similar to that in teleost divalent ion transport in the kidneys has not yet been re- ionocytes, which are localized in different parts of the vealed. The urinary bladder also serves as a site for final body [189]. water absorption before excretion in marine teleosts [134]. On the other hand, marine teleosts can absorb 70– It has been known since the early 1900s that marine 85% of ingested SW across the intestine and excrete ex- teleosts drink copiously to compensate for water lost os- cess NaCl from gill ionocytes [127, 144]. This is due to motically across the body surface [207]. The mechanisms
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